Morphological patterns in the developing vertebrate retina

Nordquist, Daniel; McLoon, Steven C.

doi:10.1007/bf01236049

Cited by 7 publications

(4 citation statements)

References 19 publications

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“…Given the comparable phenotype despite opposite orientation seen in superior coloboma patients, we hypothesized a similar etiology. Although the standard model of eye development describes an uninterrupted dorsal retina, two older studies of fish eye development identified a groove present in this space [ 18 , 19 ]. To determine if such a structure exists broadly across vertebrates and whether it is a Laminin-lined space, we chose to revisit the study of dorsal eye morphogenesis in fish, chick and mouse.…”

Section: Resultsmentioning

confidence: 99%

Morphogenetic defects underlie Superior Coloboma, a newly identified closure disorder of the dorsal eye

et al. 2018

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The eye primordium arises as a lateral outgrowth of the forebrain, with a transient fissure on the inferior side of the optic cup providing an entry point for developing blood vessels. Incomplete closure of the inferior ocular fissure results in coloboma, a disease characterized by gaps in the inferior eye and recognized as a significant cause of pediatric blindness. Here, we identify eight patients with defects in tissues of the superior eye, a congenital disorder that we term superior coloboma. The embryonic origin of superior coloboma could not be explained by conventional models of eye development, leading us to reanalyze morphogenesis of the dorsal eye. Our studies revealed the presence of the superior ocular sulcus (SOS), a transient division of the dorsal eye conserved across fish, chick, and mouse. Exome sequencing of superior coloboma patients identified rare variants in a Bone Morphogenetic Protein (Bmp) receptor (BMPR1A) and T-box transcription factor (TBX2). Consistent with this, we find sulcus closure defects in zebrafish lacking Bmp signaling or Tbx2b. In addition, loss of dorsal ocular Bmp is rescued by concomitant suppression of the ventral-specific Hedgehog pathway, arguing that sulcus closure is dependent on dorsal-ventral eye patterning cues. The superior ocular sulcus acts as a conduit for blood vessels, with altered sulcus closure resulting in inappropriate connections between the hyaloid and superficial vascular systems. Together, our findings explain the existence of superior coloboma, a congenital ocular anomaly resulting from aberrant morphogenesis of a developmental structure.

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Section: Resultsmentioning

confidence: 99%

Morphogenetic defects underlie Superior Coloboma, a newly identified closure disorder of the dorsal eye

et al. 2018

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“…In a process analogous to that seen for pattern formation in other parts of the embryo, a two-dimensional coordinate system appears to be set up relatively early, before optic cup formation (Crossland et al, 1974;Dutting and Thanos, 1995). Morphologically, notches have been described that delineate nasal, dorsal, and temporal positions early in development and suggest that the retina shows segmentation patterns analogous to other parts of the CNS (Nordquist and McLoon, 1991). The restricted expression patterns of segmentation genes Paiu2 ventrally (Nornes et al, 1990) and Writ-7b dorsally (Parr et al, 1993) support this hypothesis.…”

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confidence: 89%

Development of the pattern of photoreceptors in the chick retina

1996

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The various classes of photoreceptor cells found in vertebrate retinae are organized in specific patterns, which are important for visual function. It is not known how these patterns are achieved during development. The chick retina provides an excellent model system in which to investigate this issue, containing cone opsins red, green, blue, and violet, as well as the rod-specific opsin rhodopsin. In this study, whole-mount in situ hybridization has revealed striking differences among opsins in both spatial and temporal aspects of expression. The long-wavelength cone opsins, red and green, were first detected in a small spot within the area centralis at embryonic day 14 (E14). In contrast, the short-wavelength cone opsins, blue and violet, were not detected until 2 d later and showed domains of expression both within the area centralis and in temporal retina. The first rhodopsin transcripts were seen at E15 in inferior retina. When opsin expression was first detected, there were differences in the localization of RNA within the inner segment of cone photoreceptors, suggesting that morphological differentiation preceded the expression of photopigment molecules. Marked differences in the distribution of rods and cones were also found. Within the area centralis, a circular rod-free zone bisected by a narrow rod-sparse region along the nasal-temporal axis was evident as soon as rhodopsin RNA could be detected. Such specialized regions appear to be set aside soon after photoreceptor cells become postmitotic, as evidenced by a spatially restricted pattern of visinin RNA observed at E7. The onset of particular opsins in restricted regions of the retina suggest an underlying pattern related to visual function in the chick.

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“…The apical aspect of the retinal epithelium contains progenitor cells that proliferate and generate the neurons and glia of the neural retina (Nordquist and McLoon, 1991). Neurogenesis begins in the central retina and progresses to more peripheral regions over the course of several days (Mey and Thanos, 1992).…”

Section: Retinal Development and Rxr␥ Gene Expressionmentioning

confidence: 99%

Retinoid X receptor ? gene transcripts are expressed by a subset of early generated retinal cells and eventually restricted to photoreceptors

Hoover

Seleiro²,

Kielland

et al. 1998

J. Comp. Neurol.

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We have examined the distribution of the retinoid X receptor gamma (RXRgamma) in the developing chicken retina by using in situ hybridization and RNase protection assays. We detected RXRgamma transcripts as early as 4 days of embryonic development (d4) in central regions of the retina, spreading to more peripheral regions by d8. The first few RXRgamma-positive cells were scattered within the depth of the retinal neuroepithelium, but as they increased in number they became localized predominantly to the apical (outer, ventricular) layer. The identity of the RXRgamma-positive cells at these stages is unknown, due to the lack of cell type-specific markers. By d10, when photoreceptors and ganglion cells have been generated and begun to establish their definitive layers, RXRgamma-positive cells were virtually restricted to the photoreceptor layer, and maintained this distribution to posthatch stages. RNase protection assays were performed on whole retinae to verify the temporal pattern of in situ hybridization results and showed that between d5 and d16 there was a significant increase in the mRNA levels of the RXRgamma2 isoform. Between d16 and early posthatch stages the level of RXRgamma2 mRNA did not change significantly. Consistent with previous studies, mRNA levels of the RXRgamma1 isoform were substantially lower than mRNA levels of the RXRgamma2 isoform at all time points examined. These results demonstrate that RXRgamma mRNA is expressed in photoreceptors in the developing chicken retina and implicate RXRgamma as the earliest marker of photoreceptor differentiation documented to date.

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Morphological patterns in the developing vertebrate retina

Cited by 7 publications

References 19 publications

Morphogenetic defects underlie Superior Coloboma, a newly identified closure disorder of the dorsal eye

Morphogenetic defects underlie Superior Coloboma, a newly identified closure disorder of the dorsal eye

Development of the pattern of photoreceptors in the chick retina

Retinoid X receptor ? gene transcripts are expressed by a subset of early generated retinal cells and eventually restricted to photoreceptors

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